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Evolution without sex is predicted to impact genomes in numerous ways. Case studies of individual parthenogenetic animals have reported peculiar genomic features that were suggested to be caused by their mode of reproduction, including high heterozygosity, a high abundance of horizontally acquired genes, a low transposable element load, or the presence of palindromes. We systematically characterized these genomic features in published genomes of 26 parthenogenetic animals representing at least 18 independent transitions to asexuality. Surprisingly, not a single feature was systematically replicated across a majority of these transitions, suggesting that previously reported patterns were lineage-specific rather than illustrating the general consequences of parthenogenesis. We found that only parthenogens of hybrid origin were characterized by high heterozygosity levels. Parthenogens that were not of hybrid origin appeared to be largely homozygous, independent of the cellular mechanism underlying parthenogenesis. Overall, despite the importance of recombination rate variation for the evolution of sexual animal genomes, the genome-wide absence of recombination does not appear to have had the dramatic effects which are expected from classical theoretical models. The reasons for this are probably a combination of lineage-specific patterns, the impact of the origin of parthenogenesis, and a survivorship bias of parthenogenetic lineages.

Finding a partner and having sex to produce babies is a common way to reproduce. Yet, upon closer look, we see that nature provides many ways for reproduction. What about a world without males? What first sounds impossible is the reality for many organisms that reproduce asexually, meaning without having sex. Females produce daughters that are clones of themselves, so no partner is required and males are dispensable. An Example of such all-female societies are several species of oribatid mites, which live in soils. These mites were already on earth long before the dinosaurs. Have oribatid mites always been asexual? Why do they reproduce without males? Does asexual reproduction have any advantages? Keep reading to learn about asexual reproduction and why oribatid mites are a key organism to investigate the question, “Why sex?”.

International audience; Sex strongly impacts genome evolution via recombination and segregation. In the absence of these processes, haplotypes within lineages of diploid organisms are predicted to accumulate mutations independently of each other and diverge over time. This so-called “Meselson effect” is regarded as a strong indicator of the long-term evolution under obligate asexuality. Here, we present genomic and transcriptomic data of three populations of the asexual oribatid mite species Oppiella nova and its sexual relative Oppiella subpectinata . We document strikingly different patterns of haplotype divergence between the two species, strongly supporting Meselson effect–like evolution and long-term asexuality in O. nova : I) variation within individuals exceeds variation between populations in O. nova but vice versa in O. subpectinata ; II) two O. nova sublineages feature a high proportion of lineage-specific heterozygous single-nucleotide polymorphisms (SNPs), indicating that haplotypes continued to diverge after lineage separation; III) the deepest split in gene trees generally separates the two haplotypes in O. nova , but populations in O. subpectinata ; and IV) the topologies of the two haplotype trees match each other. Our findings provide positive evidence for the absence of canonical sex over evolutionary time in O. nova and suggest that asexual oribatid mites can escape the dead-end fate usually associated with asexual lineages.

Significance Putatively ancient asexual species pose a challenge to theory because they appear to escape the predicted negative long-term consequences of asexuality. Although long-term asexuality is difficult to demonstrate, specific signatures of haplotype divergence, called the “Meselson effect,” are regarded as strong support for long-term asexuality. Here, we provide evidence for the Meselson effect in an asexual oribatid mite species, Oppiella nova, and we show that the effect is not caused by hybridization or polyploidization. Our findings provide conclusive evidence for the long-term absence of sex in O. nova and suggest that asexual oribatid mites can escape the dead-end fate usually associated with asexual reproduction., Sex strongly impacts genome evolution via recombination and segregation. In the absence of these processes, haplotypes within lineages of diploid organisms are predicted to accumulate mutations independently of each other and diverge over time. This so-called “Meselson effect” is regarded as a strong indicator of the long-term evolution under obligate asexuality. Here, we present genomic and transcriptomic data of three populations of the asexual oribatid mite species Oppiella nova and its sexual relative Oppiella subpectinata. We document strikingly different patterns of haplotype divergence between the two species, strongly supporting Meselson effect–like evolution and long-term asexuality in O. nova: I) variation within individuals exceeds variation between populations in O. nova but vice versa in O. subpectinata; II) two O. nova sublineages feature a high proportion of lineage-specific heterozygous single-nucleotide polymorphisms (SNPs), indicating that haplotypes continued to diverge after lineage separation; III) the deepest split in gene trees generally separates the two haplotypes in O. nova, but populations in O. subpectinata; and IV) the topologies of the two haplotype trees match each other. Our findings provide positive evidence for the absence of canonical sex over evolutionary time in O. nova and suggest that asexual oribatid mites can escape the dead-end fate usually associated with asexual lineages.

International audience; Ostracods are one of the oldest crustacean groups with an excellent fossil record and high importance for phylogenetic analyses but genome resources for this class are still lacking. We have successfully assembled and annotated the first reference genomes for three species of nonmarine ostracods; two with obligate sexual reproduction (Cyprideis torosa and Notodromas monacha) and the putative ancient asexual Darwinula stevensoni. This kind of genomic research has so far been impeded by the small size of most ostracods and the absence of genetic resources such as linkage maps or BAC libraries that were available for other crustaceans. For genome assembly, we used an Illumina-based sequencing technology, resulting in assemblies of similar sizes for the three species (335-382 Mb) and with scaffold numbers and their N50 (19-56 kb) in the same orders of magnitude. Gene annotations were guided by transcriptome data from each species. The three assemblies are relatively complete with BUSCO scores of 92-96. The number of predicted genes (13,771-17,776) is in the same range as Branchiopoda genomes but lower than in most malacostracan genomes. These three reference genomes from nonmarine ostracods provide the urgently needed basis to further develop ostracods as models for evolutionary and ecological research.

Sex strongly impacts genome evolution via recombination and segregation. In the absence of these processes, haplotypes within lineages of diploid organisms are predicted to accumulate mutations independently of each other and diverge over time. This so-called ‘Meselson effect’ is regarded as a strong indicator of the long-term evolution under obligate asexuality. Here, we present genomic and transcriptomic data of three populations of the asexual oribatid mite speciesOppiella novaand its sexual relativeOppiella subpectinata. We document strikingly different patterns of haplotype divergence between the two species, strongly supporting Meselson effect like evolution and ancient asexuality inO. nova: (I) Variation within individuals exceeds variation between populations inO. novabutvice versainO. subpectinata. (II) TwoO. novasub-lineages feature a high proportion of heterozygous genotypes and lineage-specific haplotypes, indicating that haplotypes diverged independently within the two lineages after their split. (III) The deepest split in gene trees generally separates haplotypes inO. nova, but populations inO. subpectinata. (IV) Tree topologies of the two haplotypes match each other. Our findings provide positive evidence for the absence of sex over evolutionary time inO. novaand suggest that asexual oribatid mites can escape the dead-end fate usually associated with asexual lineages.

The shift from sexual reproduction to parthenogenesis has occurred repeatedly in animals, but how the loss of sex affects genome evolution remains poorly understood. We generated de novo reference genomes for five independently evolved parthenogenetic species in the stick insect genus Timema and their closest sexual relatives. Using these references in combination with population genomic data, we show that parthenogenesis results in an extreme reduction of heterozygosity, and often leads to genetically uniform populations. We also find evidence for less effective positive selection in parthenogenetic species, supporting the view that sex is ubiquitous in natural populations because it facilitates fast rates of adaptation. Contrary to studies of non-recombining genome portions in sexual species, genomes of parthenogenetic species do not accumulate transposable elements (TEs), likely because successful parthenogens derive from sexual ancestors with inactive TEs. Because we are able to conduct replicated comparisons across five species pairs, our study reveals, for the first time, how animal genomes evolve in the absence of sex in natural populations, providing empirical support for the negative consequences of parthenogenetic reproduction as predicted by theory.

Asexual reproduction has evolved repeatedly from sexual ancestors across a wide range of taxa. While the costs and benefits associated with asexuality have received considerable attention, the molecular changes underpinning the evolution of asexual reproduction remain relatively unexplored. In particular, it is completely unknown whether the repeated evolution of asexual phenotypes involves similar molecular changes, as previous studies have focused on changes occurring in single lineages. Here we investigate the extent of convergent gene expression changes across five independent transitions to asexuality in stick insects. We compared gene expression of asexual females to females of close sexual relatives in whole-bodies, reproductive tracts, and legs. We identified a striking amount of convergent gene expression change (up to 8% of genes), greatly exceeding that expected by chance. Convergent changes were also tissue-specific, and most likely driven by selection for functional changes. Genes showing convergent changes in the reproductive tract were associated with meiotic spindle formation and centrosome organization. These genes are particularly interesting as they can influence the production of unreduced eggs, a key barrier to asexual reproduction. Changes in legs and whole-bodies were likely involved in female sexual trait decay, with enrichment in terms such as sperm-storage and pigmentation. By identifying changes occurring across multiple independent transitions to asexuality, our results provide a rare insight into the molecular basis of asexual phenotypes and suggest that the evolutionary path to asexuality is highly constrained, requiring repeated changes to the same key genes.

The predominance of sex in eukaryotes is still enigmatic. Sex, a composed process of meiosis and mixis cycles, confers high costs but the selective advantages remain unclear. In this review, we focus on potentially detrimental effects of asexuality on genome evolution. Theory predicts that asexual lineages should suffer from lack of meiotic DNA repair, accumulation of deleterious mutations, proliferation of transposable elements, among others. Here, we compare the different genomic features, life cycles, developmental pathways, and cytological mechanisms in the major eukaryotic groups, i.e., in protists, animals, fungi, and plants. In general, it is difficult to disentangle lineage-specific features from general features of asexuality. In all groups, forms of asexuality are predominantly facultative or cyclical. A variety of mixed or partial sexual developmental pathways exists, maintaining some components of sexuality, while obligate asexuality appears to be rare in eukaryotes. The strongest theoretical prediction for negative consequences of asexuality is decreased effectiveness of selection compared to sexuality. While some studies have shown increased rates of mutation accumulation in asexuals, others using whole-genome comparisons did not find this pattern. Various mechanisms exist that can alleviate the negative consequences of accumulation of negative mutations. More empirical data are needed to understand comprehensively the role of genome evolution for the maintenance of sex.

BackgroundParasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biocontrol, and infecting aphids requires overcoming both aphid defenses and their defensive endosymbionts.ResultsWe present thede novogenome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids:Aphidius erviandLysiphlebus fabarum(Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp), highly syntenic, and the most AT-rich reported thus far for any arthropod (GC content: 25.8% and 23.8%). This nucleotide bias is accompanied by skewed codon usage, and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and age-specific energy demands. We identify expansions of F-box/Leucine-rich-repeat proteins, suggesting that diversification in this gene family may be associated with their broad host range or with countering defenses from aphids’ endosymbionts. The absence of some immune genes (Toll and Imd pathways) resembles similar losses in their aphid hosts, highlighting the potential impact of symbiosis on both aphids and their parasitoids.ConclusionsThese findings are of fundamental interest for insect evolution and beyond. This will provide a strong foundation for further functional studies including coevolution with respect to their hosts, the basis of successful infection, and biocontrol. Both genomes are available athttps://bipaa.genouest.org.

Males and females feature strikingly different phenotypes, despite sharing most of their genome. The resolution of this apparent paradox is through differential gene expression, whereby genes are expressed at different levels in each sex. This resolution, however, is likely to be incomplete, leading to conflict between males and females over the optimal expression of genes. We test the hypothesis that gene expression in females is constrained from evolving to its optimum level due to sexually antagonistic selection on males, by examining changes sex-biased gene expression in five obligate asexual species of stick insect, which do not produce males. We predicted that the transcriptome of asexual females would be feminized as asexual females do not experience any sexual conflict. Contrary to our prediction we find that asexual females feature masculinized gene expression, and hypothesise that this is due to shifts in female optimal gene expression levels following the suppression of sex.

Transposable elements (TEs) are able to proliferate in genomes via different self-copying mechanisms. Theory predicts that sexual reproduction can both facilitate and restrain TE accumulation by respectively providing TEs with a means of spreading to all individuals in a population and facilitating TE load reduction via purifying selection. By quantifying genomic TE loads over time in experimental sexual and asexual yeast populations, we provide direct evidence that asexual reproduction drives a reduction of genomic TE loads. We show, using simulations, that this reduction occurs via evolution of TE activity, most likely via increased excision rates. Our study thus demonstrates that sexual reproduction is a major driver of TE loads and at the root of the success of TEs.

Evolution without sex is predicted to impact genomes in numerous ways. Case studies of individual parthenogenetic animals have reported peculiar genomic features which were suggested to be caused by their mode of reproduction, including high heterozygosity, a high abundance of horizontally acquired genes, a low transposable element load, or the presence of palindromes. We systematically characterized these genomic features in published genomes of 26 parthenogenetic animals representing at least 18 independent transitions to asexuality. Surprisingly, not a single feature was systematically replicated across a majority of these transitions, suggesting that previously reported patterns were lineage specific rather than illustrating general consequences of parthenogenesis. We found that only parthenogens of hybrid origin were characterized by high heterozygosity levels. Parthenogens that were not of hybrid origin appeared to be largely homozygous, independently of the cellular mechanism underlying parthenogenesis. Overall, despite the importance of recombination rate variation for the evolution of sexual animal genomes, the genome-wide absence of recombination does not appear to have had the dramatic effects which are expected from classical theoretical models. The reasons for this are probably a combination of lineage-specific patterns, impact of the origin of parthenogenesis, and a survivorship bias of parthenogenetic lineages.

International audience; Recombination is a fundamental process with significant impacts on genome evolution. Predicted consequences of the loss of recombination include a reduced effectiveness of selection, changes in the amount of neutral polymorphisms segregating in populations, and an arrest of GC-biased gene conversion. Although these consequences are empirically well documented for nonrecombining genome portions, it remains largely unknown if they extend to the whole genome scale in asexual organisms. We identify the consequences of asexuality using de novo transcriptomes of five independently derived, obligately asexual lineages of stick insects, and their sexual sister-species. We find strong evidence for higher rates of deleterious mutation accumulation, lower levels of segregating polymorphisms and arrested GC-biased gene conversion in asexuals as compared with sexuals. Taken together, our study conclusively shows that predicted consequences of genome evolution under asexuality can indeed be found in natural populations.

Sex is beneficial in the long term because it can prevent mutational meltdown through increased effectiveness of selection. This idea is supported by empirical evidence of deleterious mutation accumulation in species with a recent transition to asexuality. Here, we study the effectiveness of purifying selection in oribatid mites which have lost sex millions of years ago and diversified into different families and species while reproducing asexually. We compare the accumulation of deleterious nonsynonymous and synonymous mutations between three asexual and three sexual lineages using transcriptome data. Contrasting studies of young asexual lineages, we find evidence for strong purifying selection that is more effective in asexual as compared to sexual oribatid mite lineages. Our results suggest that large populations likely sustain effective purifying selection and facilitate the escape of mutational meltdown in the absence of sex. Thus, sex per se is not a prerequisite for the long-term persistence of animal lineages., Asexual reproduction is thought to be an evolutionary dead end in eukaryotes because deleterious mutations will not be purged effectively. Here, Brandt and colleagues show that anciently asexual oribatid mites in fact have reduced accumulation of deleterious mutations compared to their sexual relatives.

Stick to the Bush Can the underlying genetic changes driving the divergence of populations into new species be predicted or repeated? Soria-Carrasco et al. (p. 738 ) investigated the genetic changes observed after one generation when stick insect ( Timema cristinae ) populations were transplanted from their preferred host plants to alternative hosts. Diverged genetic regions were relatively small, with most loci showing divergence in a single population pair. However, the number of loci showing parallel divergence was greater than expected by chance. Thus, selection can drive parallel phenotypic evolution via parallel genetic changes.

The mode of reproduction has been predicted to affect the proliferation of transposable elements (TEs). A population that switches from sexual to asexual reproduction could either accumulate TEs because purifying selection becomes less efficient, or a decrease in TE load because the opportunity for horizontal transmission is reduced. A third possibility is that the mechanism that induces asexual reproduction affects TE dynamics as a side effect. We propose two such mechanisms that might explain recently described patterns of TE abundance in sexual and asexual lineages of the parasitoid wasp Leptopilina clavipes. Asexual reproduction in this species is induced by endosymbiotic Wolbachia bacteria. In order to achieve parthenogenesis in its host, Wolbachia might remove methylation or interfere with Argonaute proteins. Both methylation and Argonaute proteins are known to control TE activity in other species. By interfering with either, Wolbachia might therefore secondarily hamper the control of specific TEs.

Transposable elements (TEs) and other repetitive DNA can accumulate in the absence of recombination, a process contributing to the degeneration of Y-chromosomes and other nonrecombining genome portions. A similar accumulation of repetitive DNA is expected for asexually reproducing species, given their entire genome is effectively nonrecombining. We tested this expectation by comparing the whole-genome TE loads of five asexual arthropod lineages and their sexual relatives, including asexual and sexual lineages of crustaceans (Daphnia water fleas), insects (Leptopilina wasps), and mites (Oribatida). Surprisingly, there was no evidence for increased TE load in genomes of asexual as compared to sexual lineages, neither for all classes of repetitive elements combined nor for specific TE families. Our study therefore suggests that nonrecombining genomes do not accumulate TEs like nonrecombining genomic regions of sexual lineages. Even if a slight but undetected increase of TEs were caused by asexual reproduction, it appears to be negligible compared to variance between species caused by processes unrelated to reproductive mode. It remains to be determined if molecular mechanisms underlying genome regulation in asexuals hamper TE activity. Alternatively, the differences in TE dynamics between nonrecombining genomes in asexual lineages versus nonrecombining genome portions in sexual species might stem from selection for benign TEs in asexual lineages because of the lack of genetic conflict between TEs and their hosts and/or because asexual lineages may only arise from sexual ancestors with particularly low TE loads. peerReviewed

The maintenance of sex is the 'queen of problems' in evolutionary biology. This article elucidates the diversity and distribution of reproductive modes and explains current theories that propose mechanisms through which sexual reproduction can provide benefits. This article further illustrates empirical evidence for different theories from the laboratory and natural systems.

Loss of sexual reproduction is considered an evolutionary dead end for metazoans, but bdelloid rotifers challenge this view as they appear to have persisted asexually for millions of years1. Neither male sex organs nor meiosis have ever been observed in these microscopic animals: oocytes are formed through mitotic divisions, with no reduction of chromosome number and no indication of chromosome pairing2. However, current evidence does not exclude that they may engage in sex on rare, cryptic occasions. Here we report the genome of a bdelloid rotifer, Adineta vaga (Davis, 1873)3, and show that its structure is incompatible with conventional meiosis. At gene scale, the genome of A. vaga is tetraploid and comprises both anciently duplicated segments and less divergent allelic regions. However, in contrast to sexual species, the allelic regions are rearranged and sometimes even found on the same chromosome. Such structure does not allow meiotic pairing; instead, we find abundant evidence of gene conversion, which may limit the accumulation of deleterious mutations in the absence of meiosis. Gene families involved in resistance to oxidation, carbohydrate metabolism and defence against transposons are significantly expanded, which may explain why transposable elements cover only 3% of the assembled sequence. Furthermore, 8% of the genes are likely to be of non-metazoan origin and were probably acquired horizontally. This apparent convergence between bdelloids and prokaryotes sheds new light on the evolutionary significance of sex., National Science Foundation (U.S.) (grant MCB-0821956), National Science Foundation (U.S.) (NSF grant MCB-1121334), German Research Foundation (grant HA 5163/2-1), Ministry of Education and Science of the Russian Federation (grant 11.G34.31.0008), National Science Foundation (U.S.) (NSF CAREER grant number 0644282), National Science Foundation (U.S.) (NSF grant MCB-0923676), Belgian National Foundation for Scientific Research (FRFC grant 2.4.655.09.F), University of Namur (start-up grant)

Trait loss is a widespread phenomenon with pervasive consequences for a species’ evolutionary potential. The genetic changes underlying trait loss have only been clarified in a small number of cases. None of these studies can identify whether the loss of the trait under study was a result of neutral mutation accumulation or negative selection. This distinction is relatively clear-cut in the loss of sexual traits in asexual organisms. Male-specific sexual traits are not expressed and can only decay through neutral mutations, whereas female-specific traits are expressed and subject to negative selection. We present the genome of an asexual parasitoid wasp and compare it to that of a sexual lineage of the same species. We identify a short-list of 16 genes for which the asexual lineage carries deleterious SNP or indel variants, whereas the sexual lineag e does not. Using tissue-specific expression data from other insects, we show that fifteen of these are expressed in male-specific reproductive tissues. Only one deleterious variant was found that is expressed in the female-specific spermathecae, a trait that is heavily degraded and thought to be under negative selection in L. clavipes . Although the phenotypic decay of male-specific sexual traits in asexuals is generally slow compared with the decay of female-specific sexual traits, we show that male-specific traits do indeed accumulate deleterious mutations as expected by theory. Our results provide an excellent starting point for detailed s tudy of the genomics of neutral and selected trait decay.